Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments
Abstract During tissue invasion individual tumor cells exhibit two interconvertible migration modes, namely mesenchymal and amoeboid migration. The cellular microenvironment triggers the switch between both modes, thereby allowing adaptation to dynamic conditions. It is, however, unclear if this amo...
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Nature Portfolio
2017
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oai:doaj.org-article:ac30830f1fea4192b35fc976d9691ea02021-12-02T11:52:35ZAmoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments10.1038/s41598-017-09300-32045-2322https://doaj.org/article/ac30830f1fea4192b35fc976d9691ea02017-08-01T00:00:00Zhttps://doi.org/10.1038/s41598-017-09300-3https://doaj.org/toc/2045-2322Abstract During tissue invasion individual tumor cells exhibit two interconvertible migration modes, namely mesenchymal and amoeboid migration. The cellular microenvironment triggers the switch between both modes, thereby allowing adaptation to dynamic conditions. It is, however, unclear if this amoeboid-mesenchymal migration plasticity contributes to a more effective tumor invasion. We address this question with a mathematical model, where the amoeboid-mesenchymal migration plasticity is regulated in response to local extracellular matrix resistance. Our numerical analysis reveals that extracellular matrix structure and presence of a chemotactic gradient are key determinants of the model behavior. Only in complex microenvironments, if the extracellular matrix is highly heterogeneous and a chemotactic gradient directs migration, the amoeboid-mesenchymal migration plasticity allows a more widespread invasion compared to the non-switching amoeboid and mesenchymal modes. Importantly, these specific conditions are characteristic for in vivo tumor invasion. Thus, our study suggests that in vitro systems aiming at unraveling the underlying molecular mechanisms of tumor invasion should take into account the complexity of the microenvironment by considering the combined effects of structural heterogeneities and chemical gradients on cell migration.Katrin TalkenbergerElisabetta Ada Cavalcanti-AdamAnja Voss-BöhmeAndreas DeutschNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 7, Iss 1, Pp 1-12 (2017) |
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Medicine R Science Q Katrin Talkenberger Elisabetta Ada Cavalcanti-Adam Anja Voss-Böhme Andreas Deutsch Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
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Abstract During tissue invasion individual tumor cells exhibit two interconvertible migration modes, namely mesenchymal and amoeboid migration. The cellular microenvironment triggers the switch between both modes, thereby allowing adaptation to dynamic conditions. It is, however, unclear if this amoeboid-mesenchymal migration plasticity contributes to a more effective tumor invasion. We address this question with a mathematical model, where the amoeboid-mesenchymal migration plasticity is regulated in response to local extracellular matrix resistance. Our numerical analysis reveals that extracellular matrix structure and presence of a chemotactic gradient are key determinants of the model behavior. Only in complex microenvironments, if the extracellular matrix is highly heterogeneous and a chemotactic gradient directs migration, the amoeboid-mesenchymal migration plasticity allows a more widespread invasion compared to the non-switching amoeboid and mesenchymal modes. Importantly, these specific conditions are characteristic for in vivo tumor invasion. Thus, our study suggests that in vitro systems aiming at unraveling the underlying molecular mechanisms of tumor invasion should take into account the complexity of the microenvironment by considering the combined effects of structural heterogeneities and chemical gradients on cell migration. |
format |
article |
author |
Katrin Talkenberger Elisabetta Ada Cavalcanti-Adam Anja Voss-Böhme Andreas Deutsch |
author_facet |
Katrin Talkenberger Elisabetta Ada Cavalcanti-Adam Anja Voss-Böhme Andreas Deutsch |
author_sort |
Katrin Talkenberger |
title |
Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
title_short |
Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
title_full |
Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
title_fullStr |
Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
title_full_unstemmed |
Amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
title_sort |
amoeboid-mesenchymal migration plasticity promotes invasion only in complex heterogeneous microenvironments |
publisher |
Nature Portfolio |
publishDate |
2017 |
url |
https://doaj.org/article/ac30830f1fea4192b35fc976d9691ea0 |
work_keys_str_mv |
AT katrintalkenberger amoeboidmesenchymalmigrationplasticitypromotesinvasiononlyincomplexheterogeneousmicroenvironments AT elisabettaadacavalcantiadam amoeboidmesenchymalmigrationplasticitypromotesinvasiononlyincomplexheterogeneousmicroenvironments AT anjavossbohme amoeboidmesenchymalmigrationplasticitypromotesinvasiononlyincomplexheterogeneousmicroenvironments AT andreasdeutsch amoeboidmesenchymalmigrationplasticitypromotesinvasiononlyincomplexheterogeneousmicroenvironments |
_version_ |
1718395004080095232 |